Understanding the evolutionary processes that influence fitness is critical to predicting species' responses to selection. Interactions among evolutionary processes including gene flow, drift and the strength of selection can lead to either local adaptation or maladaptation especially in heterogeneous landscapes. Populations experiencing novel environments or resources are ideal for understanding the mechanisms underlying adaptation or maladaptation, specifically in locally co-evolved interactions. We used the interaction between a native herbivore that oviposits on a patchily distributed introduced plant that in turn causes significant mortality to the larvae to test for signatures of local adaptation in areas where the two co-occurred. We used whole genome sequencing to explore population structure, patterns of gene flow and signatures of local adaptation. We found signatures of local adaptation in response to the introduced plant in the absence of strong population structure with no genetic differentiation and low genetic variation. Additionally, we found localized allele frequency differences within a single population between habitats with and without the lethal plant, highlighting the effects of strong selection. Our work highlights the potential for adaptation to occur in a fine-grained landscape in the presence of gene flow and low genetic variation.